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The scale of landscape effect on seed dispersal depends on both response variables and landscape predictor

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Abstract

Context

Landscape structure can affect seed dispersal, but the spatial scale at which such effect is maximized (scale of effect, SoE) is unknown.

Objectives

We assessed patterns and predictors of SoE on the seed rain in two Mexican regions: the relatively well-preserved Lacandona rainforest, and the more deforested Los Tuxtlas rainforest. We hypothesized that source limitation at Los Tuxtlas makes seed dispersal more reliant on landscape patterns measured across larger spatial scales, especially when considering connectedness-related landscape metrics and dispersal-dependent responses.

Methods

We recorded the abundance and diversity of tree seeds in 20 forest sites per region, separately assessing local (dropping from neighboring trees) and dispersed (immigrant) seeds. We measured forest cover, fragmentation, and matrix openness in 11 concentric landscapes surrounding each site and tested for differences in SoE among regions, landscape metrics, response variables, and seed origins.

Results

Contrary to expectations, SoE did not differ between regions and seed origins. Yet, as expected, forest cover tended to have larger SoE than matrix openness, with fragmentation showing intermediate values. Response variables also followed the predicted SoE pattern (abundance < diversity < species richness).

Conclusions

Forest cover has larger SoE than matrix openness, possibly because forest cover is related to large-scale processes (e.g. long-distance dispersal) and matrix openness may drive small-scale processes (e.g. edge effects). Species richness may have larger SoE because of its dependence on long-distance dispersal. Therefore, to accurately assess the effect of landscape structure on seed dispersal, the optimal scale of analysis depends on predictor and response variables.

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References

  • Arroyo-Rodríguez V, Mandujano S, Benítez-Malvido J (2008) Landscape attributes affecting patch occupancy by howler monkeys (Alouatta palliata mexicana) at Los Tuxtlas, Mexico. Am J Primatol 70:69–77

    Article  PubMed  Google Scholar 

  • Arroyo-Rodríguez V, Águilar-Barajas E, González-Zamora A, Rocha-Ramírez V, González-Rodríguez A, Oyama K (2017a) Parent-parent and parent-offspring distances in Spondias radlkoferi seeds suggest long-distance pollen and seed dispersal: evidence from latrines of the spider monkey. J Trop Ecol 33:95–106

    Article  Google Scholar 

  • Arroyo-Rodríguez V, Melo F, Martínez-Ramos M et al (2017b) Multiple successional pathways in human-modified tropical landscapes: New insights from forest succession, forest fragmentation and landscape ecology research. Biol Rev 92:326–340

    Article  PubMed  Google Scholar 

  • Arroyo-Rodríguez V, Saldaña-Vázquez RA, Fahrig L, Santos BA (2017c) Does forest fragmentation cause an increase in forest temperature? Ecol Res 32:81–88

    Article  Google Scholar 

  • Boesing AL, Nichols E, Metzger JP (2018) Biodiversity extinction thresholds are modulated by matrix type. Ecography 41:1520–1533

    Article  Google Scholar 

  • Carabias J, De la Maza J, Cadena R (2015) Conservación y desarrollo sustentable en la selva Lacandona: 25 años de actividades y experiencias. Natura y Ecosistemas Mexicanos A.C., Mexico City

    Google Scholar 

  • Carrara E, Arroyo-Rodríguez V, Vega-Rivera JH, Schondube JE, Freitas SM, Fahrig L (2015) Impact of landscape composition and configuration on forest specialist and generalist bird species in the fragmented Lacandona rainforest, Mexico. Biol Conserv 184:117–126

    Article  Google Scholar 

  • Chao A, Jost L (2012) Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93:2533–2547

    Article  PubMed  Google Scholar 

  • Chao A, Shen TJ (2010) Program SPADE: species prediction and diversity estimation. Program and user’s guide. CARE, Hsin-Chu

    Google Scholar 

  • Chaves OM, Stoner KE, Arroyo-Rodríguez V (2011) Seasonal differences in activity patterns of Geoffroyi´s spider monkeys (Ateles geoffroyi) living in continuous and fragmented forests in southern Mexico. Int J Primatol 32:960–973

    Article  Google Scholar 

  • Clark CJ, Poulsen JR, Bolker BM, Connor EF, Parker VT (2005) Comparative seed shadows of bird-, monkey-, and wind-dispersed trees. Ecology 86:2684–2694

    Article  Google Scholar 

  • Crawley MJ (2007) Statistical modelling in the R book. John Wiley & Sons Ltd, Chichester, UK

    Google Scholar 

  • Dirzo R, Miranda A (1990) Contemporary neotropical defaunation and forest structure, function, and diversity—a sequel to John Terborgh. Conserv Biol 4:444–447

    Article  Google Scholar 

  • Dunning J, Danielson B, Pulliam H (1992) Ecological processes that affect populations in complex landscapes. Oikos 65:169–175

    Article  Google Scholar 

  • Eigenbrod F, Hecnar SJ, Fahrig L (2011) Sub-optimal study design has major impacts on landscape-scale inference. Biol Conserv 144:298–305

    Article  Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515

    Article  Google Scholar 

  • Fahrig L (2007) Non-optimal animal movement in human-altered landscapes. Func Ecol 21:1003–1015

    Article  Google Scholar 

  • Fahrig L (2013) Rethinking patch size and isolation effects: the habitat amount hypothesis. J Biogeogr 40:1649–1663

    Article  Google Scholar 

  • Fahrig L (2017) Ecological responses to habitat fragmentation per se. Annu Rev Ecol Evol Syst 48:1–23

    Article  Google Scholar 

  • Fortin M-J, Dale MRT, ver Hoef J (2002) Spatial analysis in ecology. In: El-Shaarawi A, Piegorsch WW (eds) Encyclopedia of environmetrics. Wiley, Chichester, pp 2051–2058

    Google Scholar 

  • Galindo-González J, Sosa VJ (2003) Frugivourus bats in isolated trees and riparian vegetation associated with human-made pasture in a fragmented tropical landscape. Southwest Nat 48:579–589

    Article  Google Scholar 

  • Garmendia A, Arroyo-Rodríguez V, Estrada A, Naranjo EJ, Stoner KE (2013) Landscape and patch attributes impacting medium- and large-sized terrestrial mammals in a fragmented rain forest. J Trop Ecol 29:331–344

    Article  Google Scholar 

  • Godoy JA, Jordano P (2001) Seed dispersal by animals: exact identification of source trees with endocarp DNA microsatellites. Mol Ecol 10:2275–2283

    Article  CAS  PubMed  Google Scholar 

  • Guevara S, Laborde J (1993) Monitoring seed dispersal at isolated standing trees in tropical pastures: consequences for local species availability. Vegetatio 107(108):319–338

    Google Scholar 

  • Guevara S, Laborde J, Sánchez-Rios G (2004) Los Tuxtlas. El Paisaje de la Sierra. Instituto de Ecología, A.C., Xalapa

    Google Scholar 

  • Herrera JM, García D (2010) Effects of forest fragmentation on seed dispersal and seedling establishment in ornithochorous trees. Conserv Biol 24:1089–1098

    Article  PubMed  Google Scholar 

  • Herrera JM, Morales JM, García D (2011) Differential effects of fruit availability and habitat cover for frugivore-mediated seed dispersal in a heterogeneous landscape. J Ecol 99:1100–1107

    Article  Google Scholar 

  • Holbroock KM (2011) Home range and movement patterns of toucans: implications for seed dispersal. Biotropica 43:357–364

    Article  Google Scholar 

  • Ibarra-Manríquez G, Oyama K (1992) Ecological correlates of reproductive traits of Mexican rain forest trees. Am J Bot 79:383–394

    Article  Google Scholar 

  • Ibarra-Manríquez G, Martínez-Morales M, Cornejo-Tenorio G (2015) Frutos y semillas del bosque tropical perennifolio. Región de Los Tuxtlas, Veracruz. Comisión Nacional para el Uso y Conservación de la Biodiversidad, Mexico City

    Google Scholar 

  • Jackson HB, Fahrig L (2012) What size is a biologically relevant landscape? Landscape Ecol 27:929–941

    Article  Google Scholar 

  • Jackson HB, Fahrig L (2015) Are ecologists conducting research at the optimal scale? Glob Ecol Biogeogr 24:52–63

    Article  Google Scholar 

  • Jesus FM, Pivello VR, Meirelles AT, Franco GADC, Metzger JP (2012) The importance of landscape structure for seed dispersal in rain forest fragments. J Veg Sci 23:1126–1136

    Article  Google Scholar 

  • Jost L (2006) Entropy and diversity. Oikos 113:363–375

    Article  Google Scholar 

  • Laborde J (2004) La Reserva de la Biósfera. In: Guevara S, Laborde J, Sánchez G (eds) Los Tuxtlas. El Paisaje de la Sierra. Instituto de Ecología, A.C., Xalapa, pp 271–281

    Google Scholar 

  • Laurance WF, Ferreira LV, Rankin-de Merona JM, Laurance SG (1998) Rain forest fragmentation and the dynamics of Amazonian tree communities. Ecology 79:2032–2040

    Article  Google Scholar 

  • Laurance WF, Lovejoy T, Vasconcelos HL, Bruna EM, Didham RK, Stouffer PC, Gascon C, Bierregaard RO, Laurance SG, Sampaio E (2002) Ecosystem decay of Amazonian forest fragments: a 22 year investigation. Conserv Biol 16:605–618

    Article  Google Scholar 

  • Lehouck V, Spanhove T, Vangestel C, Cordeiro NJ, Lens L (2009) Does landscape structure affect resource tracking by avian frugivores in a fragmented Afrotropical forest? Ecography 32:789–799

    Article  Google Scholar 

  • Marcon E, Hérault B (2014) Entropart, an R package to partition diversity (http://cran.r-project.org/package=entropart)

  • Martin AE (2018) The spatial scale of a species’ response to the landscape context depends on which biological response you measure. Curr Landscape Ecol Rep 3:23–33

    Article  Google Scholar 

  • Martínez-Ramos M, Soto-Castro A (1993) Seed rain and advanced regeneration in a tropical rain forest. Vegetatio 107(108):299–318

    Google Scholar 

  • Melo FPL, Martínez E, Benítez-Malvido J, Ceballos G (2010) Forest fragmentation reduces recruitment of large seeded tree species in a semi-deciduous tropical forest of southern Mexico. J Trop Ecol 26:35–43

    Article  Google Scholar 

  • Mendoza E, Dirzo R (2007) Seed-size variation determines interspecific differential predation by mammals in a neotropical rain forest. Oikos 116:1841–1852

    Article  Google Scholar 

  • Mesquita RCG, Delamônica P, Laurance WF (1999) Effect of surrounding vegetation on edge-related tree mortality in Amazonian forest fragments. Biol Conserv 91:129–134

    Article  Google Scholar 

  • Miguet P, Jackson HB, Jackson ND, Martin AE, Fahrig L (2016) What determines the spatial extent of landscape effects on species? Landscape Ecol 31:1177–1194

    Article  Google Scholar 

  • Mora F (2008) Caracterización de la cobertura forestal en el Corredor Biológico Mesoamericano-México: patrones espaciales en la pérdida y fragmentación de los bosques. In: Importancia del capital ecológico de la región del Corredor Biológico Mesoamericano-México: evaluación de la biodiversidad, ciclo hidrológico y dinámica de la cobertura forestal. Comisión Nacional para el Uso y Conservación de la Biodiversidad, Mexico City, pp 55–84.

  • Muench C, Martínez-Ramos M (2016) Can community-protected areas conserve biodiversity in human-modified tropical landscapes? The case of terrestrial mammals in southern Mexico. Trop Conserv Sci 9:178–202

    Article  Google Scholar 

  • Naranjo E, Bodmer R (2007) Source-sink systems and conservation of hunted ungulates in the Lacandon rainforest, Mexico. Biol Conserv 138:412–420

    Article  Google Scholar 

  • Nathan R, Schurr FM, Spiegel O, Steinitz O, Trakhtenbrot A, Tsoar A (2008) Mechanisms of long-distance seed dispersal. Trends Ecol Evol 23:638–647

    Article  PubMed  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    Article  CAS  PubMed  Google Scholar 

  • Pfeifer M, Lefebvre V, Peres CA et al (2017) Creation of forest edges has a global impact on forest vertebrates. Nature 551:187–191

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pires AS, Lira PK, Fernandez FAS, Schittini GM, Oliveira LC (2002) Frequency of movements of small mammals among Atlantic Coastal forest fragments in Brazil. Biol Conserv 108:229–237

    Article  Google Scholar 

  • QGIS Development Team (2014) QGIS geographic information system. Open Source Geospatial Foundation. http://qgis.osgeo.org/en/site/

  • R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing. http://www.R-project.org/

  • Ricketts T (2001) The matrix matters: effective isolation in fragmented landscapes. Am Nat 158:87–99

    Article  CAS  PubMed  Google Scholar 

  • Ruffel J, Clout MN, Didham RK (2016) The matrix matters, but how should we manage it? Estimating the amount of high-quality matrix required to maintain biodiversity in fragmented landscapes. Ecography 40:171–178

    Article  Google Scholar 

  • Sánchez-Colón S, Flores Martínez A, Cruz-Leyva IA, Velázquez A (2009) Estado y transformación de los ecosistemas terrestres por causas humanas. In: Capital natural de México, vol. II: Estado de conservación y tendencias de cambio. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, Mexico City, pp 75–129

  • Smith AC, Fahrig L, Francis CM (2011) Landscape size affects the relative importance of habitat amount, habitat fragmentation, and matrix quality on forest birds. Ecography 34:103–113

    Article  Google Scholar 

  • Suárez-Castro AF, Simmonds JS, Mitchell MGE, Maron M, Rhodes JR (2018) The scale-dependent role of biological traits in landscape ecology: a review. Curr Landscape Ecol Rep 3:12–22

    Article  Google Scholar 

  • Taylor PD, Fahrig L, Henein K, Merriam G (1993) Connectivity is a vital element of landscape structure. Oikos 68:571–573

    Article  Google Scholar 

  • Tuff KT, Tuff T, Davies KF (2016) A framework for integrating thermal biology into fragmentation research. Ecol Lett 19:361–374

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vandermeer J, Carvajal R (2001) Metapopulation dynamics and the quality of the matrix. Am Nat 158:211–220

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to Felix Eigenbrod and two meticulous reviewers for providing substantial and constructive feedback, which significantly improved the previous versions of this manuscript. We are also grateful to the owners of the study forest patches in the Lacandona and Los Tuxtlas regions for allowing us to work in their properties. PAPIIT-DGAPA, UNAM (Project IN-204215), and Rufford Small Grants (16237-1) provided financial support. This paper constitutes a partial fulfillment of the Programa de Posgrado en Ciencias Biológicas of the Universidad Nacional Autónoma de México. M.S.J. obtained a scholarship from CONACyT, Mexico. V.A.-R. thanks PASPA-DGAPA-UNAM for funding his sabbatical stay at the Geomatics and Landscape Ecology Laboratory, Carleton University. Part of this manuscript was written while M.S.J. was on a research stay at the Integrative Ecology Group from Estación Biológica de Doñana. A. Jamangapé and S. Pérez provided field assistance. E. Martínez (MEXU national herbarium), S. Sinaca and G. Jamangapé helped with species identification. Sergio Nicasio-Arzeta digitized the maps. We also thank the support (infrastructure, logistics and administration team) provided by the Instituto de Investigaciones en Ecosistemas y Sustentabilidad, UNAM. H. Ferreira, A. Valencia and A. López provided technical support.

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Authors and Affiliations

  1. Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Antigua Carretera a Pátzcuaro 8701, ExHacienda de San José de La Huerta, 58190, Morelia, Michoacán, Mexico

    Miriam San-José, Víctor Arroyo-Rodríguez & Miguel Martínez-Ramos

  2. Integrative Ecology Group, Estación Biológica de Doñana, EBD-CSIC, Seville, Spain

    Pedro Jordano

  3. Departamento de Ecología y Recursos Naturales, Facultad de Ciencias, Universidad Nacional Autónoma de México, Av. Universidad 3000, Circuito Exterior s/n, Coyoacán, 04510, Mexico City, Mexico

    Jorge A. Meave

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  1. Miriam San-José
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  2. Víctor Arroyo-Rodríguez
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  3. Pedro Jordano
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Correspondence to Víctor Arroyo-Rodríguez.

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San-José, M., Arroyo-Rodríguez, V., Jordano, P. et al. The scale of landscape effect on seed dispersal depends on both response variables and landscape predictor. Landscape Ecol 34, 1069–1080 (2019). https://doi.org/10.1007/s10980-019-00821-y

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